Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Photoprotection of PSII in Hawaiian lobeliads from diverse light environments

Rebecca A. Montgomery A D , Guillermo Goldstein B and Thomas J. Givnish C
+ Author Affiliations
- Author Affiliations

A Department of Forest Resources, University of Minnesota, Saint Paul, MN 55108, USA.

B Department of Biology, University of Miami, Miami, FL 33124, USA.

C Department of Botany, University of Wisconsin, Madison, WI 53706, USA.

D Corresponding author. Email: rebeccam@umn.edu

Functional Plant Biology 35(7) 595-605 https://doi.org/10.1071/FP08031
Submitted: 20 February 2008  Accepted: 7 July 2008   Published: 21 August 2008

Abstract

Excess irradiance can reduce the quantum yield of photosynthesis via photoprotective energy dissipation, inactivation or downregulation of PSII. We examined variation in photoprotection as part of a study of adaptive radiation in photosynthetic light responses by Hawaiian lobeliads. We measured the maximum efficiency of PSII (Fv/Fm) and recovery of Fv/Fm after high light stress in field populations of 11 lobeliad species and in four species growing under common-garden greenhouse conditions. Species showed no difference in Fv/Fm (0.82 ± 0.02 (mean ± s.e.)) or in their ability to recover from light stress under field conditions. Average recovery was 74 ± 1.4% within 1 h of removal of the stress suggesting that all species maintain the ability to recover from high light stress, at least in the short-term. In contrast, the results from the common-garden indicate that long-term exposure to high irradiance and associated higher temperatures can cause a sustained reduction in PSII function. Species showed decreased Fv/Fm and percentage recovery as treatment irradiance increased. Fv/Fm and percentage recovery were positively related to native habitat PFD across species, suggesting that there has been a diversification in high light tolerance, with species from sunnier environments better able to avoid sustained declines in PSII function.

Additional keywords: adaptive radiation, chlorophyll fluorescence, common garden, non-photochemical quenching, photochemical reflectance index, xanthophyll-cycle pigments.


Acknowledgements

The authors gratefully acknowledge the research support provided by grant IBN-9904366 from the Ecological and Evolutionary Physiology Program of the US National Science Foundation. We thank Hawai’i Volcanoes National Park, the National Tropical Botanical Garden, the Koke’e Natural History Museum, Limahuli Garden and the University of Hawai’i Agricultural Experiment Station in Volcano for important logistical assistance. Ken Wood, Linda Pratt and Kate Reinard provided invaluable aid in locating populations of several rare species. We are deeply grateful to Wayne Souza of Kaua’i State Parks, Edwin Pettys of the Kaua’i Division of Forestry and Wildlife, David Foote and Linda Pratt of USGS Biological Resources Division, Betsy Gagné, Randy Kennedy, Bill Stormont and Jon Giffen of Hawai’i Natural Areas Reserves, Susan Cordell and Julie Denslow of USDA Forest Service and Sterling Keeley of the University of Hawai’i for their support in helping us obtain research permits and access to research facilities. Mahalo to Aubrey Kelly, Leilani Durand, Nicole Kuamo’o and Ken Wood for help and camaraderie in the field and for their commitment in helping to achieve the objectives of this research. We thank William Adams for his comments on a draft of this manuscript.


References


Adams WW III , Demmig-Adams B (1993) Energy dissipation and photoprotection in leaves of higher plants. In ‘Proceedings of the photosynthetic responses to the environment symposium, University of Hawaii.’ (Eds HY Yamamoto, CM Smith) pp. 27–36. (American Society of Plant Physiologists: Rockville, MD)

Adams WW, Demmig-Adams B, Logan BA, Barker DH, Osmond CB (1999) Rapid changes in xanthophyll cycle-dependent energy dissipation and photosystem II efficiency in two vines, Stephania japonica and Smilax australis, growing in the understory of an open Eucalyptus forest. Plant, Cell & Environment 22, 125–136.
Crossref | GoogleScholarGoogle Scholar | open url image1

Adams W, Watson A, Mueh K, Amiard V, Turgeon R, Ebbert V, Logan B, Combs A, Demmig-Adams B (2007) Photosynthetic acclimation in the context of structural constraints to carbon export from leaves. Photosynthesis Research 94, 455–466.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Barker DH, Adams WW (1997) The xanthophyll cycle and energy dissipation in differently oriented faces of the cactus Opuntia macrorhiza. Oecologia 109, 353–361.
Crossref | GoogleScholarGoogle Scholar | open url image1

Bilger W, Björkman O (1990) Role of xanthophyll cycle in photoprotection elucidated by measurements of light-induced absorbance changes, fluorescence and photosynthesis in leaves of Hedera canariensis. Photosynthesis Research 25, 173–185.
Crossref | GoogleScholarGoogle Scholar | open url image1

Björkman O, Demmig B (1987) Photon yield of O2 evolution and chlorophyll fluorescence characteristics at 77 K among vascular plants of diverse origins. Planta 170, 489–504.
Crossref | GoogleScholarGoogle Scholar | open url image1

Brugnoli E, Cona A, Lauteri M (1994) Xanthophyll cycle components and capacity for non-radiative energy dissipation in sun and shade leaves of Ligustrum ovalifolium exposed to conditions limiting photosynthesis. Photosynthesis Research 41, 451–463.
Crossref | GoogleScholarGoogle Scholar | open url image1

Carlquist S (1965) ‘Island life.’ (Natural History Press: New York)

Carlquist S (1970) ‘Hawaii: a natural history.’ (Natural History Press: New York)

Cavender-Bares J , Bazzaz FA (2004) From leaves to ecosystems: using chlorophyll fluorescence to assess photosynthesis and plant function in ecological studies. In ‘Chlorophyll fluorescence: a signature of photosynthesis’. (Eds GC Papageorgiou and Govindjee) pp. 737–755. (Kluwer Academic Publishers: Dordrecht, The Netherlands)

Chazdon RL (1988) Sunflecks and their importance to forest understory plants. Advances in Ecological Research 18, 1–63.
Crossref | GoogleScholarGoogle Scholar | open url image1

Demmig-Adams B (1998) Survey of thermal energy dissipation and pigment composition in sun and shade leaves. Plant & Cell Physiology 39, 474–482. open url image1

Demmig-Adams B, Adams WW (1996a) The role of xanthophyll cycle carotenoids in the protection of photosynthesis. Trends in Plant Science 1, 21–26.
Crossref | GoogleScholarGoogle Scholar | open url image1

Demmig-Adams B, Adams WW (1996b) Xanthophyll cycle and light stress in nature: uniform response to excess direct sunlight among higher plant species. Planta 198, 460–470.
Crossref | GoogleScholarGoogle Scholar | open url image1

Demmig-Adams B, Adams WW, Logan BA, Verhoeven AS (1995) Xanthophyll cycle-dependent energy dissipation and flexible photosystem II efficiency in plants acclimated to light stress. Australian Journal of Plant Physiology 22, 249–260. open url image1

Demmig-Adams B, Moeller DL, Logan BA, Adams WW (1998) Positive correlation between levels of retained zeaxanthin + antheraxanthin and degree of photoinhibition in shade leaves of Schefflera arboricola (Hayata) Merrill. Planta 205, 367–374.
Crossref | GoogleScholarGoogle Scholar | open url image1

Durand LZ, Goldstein G (2001) Photosynthesis, photoinhibition, and nitrogen use efficiency in native and invasive tree ferns in Hawaii. Oecologia 126, 345–354.
Crossref | GoogleScholarGoogle Scholar | open url image1

Fetene M, Nauke P, Lüttge U, Beck E (1997) Photosynthesis and photoinhibition in a tropical alpine giant rosette plant, Lobelia rhynchopetalum. The New Phytologist 137, 453–461.
Crossref | GoogleScholarGoogle Scholar | open url image1

Gamon JA, Pearcy RW (1990) Photoinhibition in Vitis californica: interactive effects of sunlight, temperature and water status. Plant, Cell & Environment 13, 267–275.
Crossref | GoogleScholarGoogle Scholar | open url image1

Gamon JA, Surfus JS (1999) Assessing leaf pigment content and activity with a reflectometer. The New Phytologist 143, 105–117.
Crossref | GoogleScholarGoogle Scholar | open url image1

Gamon JA, Serrano L, Surfus JS (1997) The photochemical reflectance index: an optical indicator of photosynthetic radiation use efficiency across species, functional types, and nutrient levels. Oecologia 112, 492–501.
Crossref | GoogleScholarGoogle Scholar | open url image1

Ganders FR, Berbee M, Pirseyedi M (2000) ITS base sequence phylogeny in Bidens (Asteraceae): evidence for the continental relatives of Hawaiian and Marquesan Bidens. Systematic Botany 25, 122–133.
Crossref | GoogleScholarGoogle Scholar | open url image1

Gillespie R (2004) Community assembly through adaptive radiation in Hawaiian spiders. Science 303, 356–359.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Gillespie RG, Croom HB, Palumbi SR (1994) Multiple origins of a spider radiation in Hawaii. Proceedings of the National Academy of Sciences of the United States of America 91, 2290–2294.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Gilmore AM , Yamamoto HY (1993) Biochemistry of xanthophyll-dependent nonradiative energy dissipation. In ‘Proceedings of the photosynthetic responses to the environment symposium, University of Hawaii’. (Eds HY Yamamoto, CM Smith) pp. 27–36. (American Society of Plant Physiologists: Rockville, MD)

Givnish TJ (Ed.) (1986) ‘On the economy of plant form and function.’ (Cambridge University Press: Cambridge)

Givnish TJ (1998) Adaptive plant evolution on islands: classical patterns, molecular data, new insights. In ‘Evolution on Islands’. (Ed. PR Grant) pp. 281–304. (Oxford University Press: Oxford)

Givnish TJ , Sytsma KJ , Hahn WJ , Smith JF (1995) Molecular evolution, adaptive radiation, and geographic species in Cyanea (Campanulaceae, Lobelioideae). In ‘Hawaiian biogeography: evolution on a hot spot archipelago’. (Eds WL Wagner, VA Funk) pp. 288–337. (Smithsonian Institution Press: Washington)

Givnish TJ, Montgomery RA, Goldstein G (2004) Adaptive radiation of photosynthetic physiology in the Hawaiian lobeliads: light regimes, static light responses, and whole-plant compensation points. American Journal of Botany 91, 228–246.
Crossref | GoogleScholarGoogle Scholar | open url image1

Grace J, Nichol C, Disney M, Lewis P, Quaife T, Bowyer P (2007) Can we measure terrestrial photosynthesis from space directly, using spectral reflectance and fluorescence? Global Change Biology 13, 1484–1497.
Crossref | GoogleScholarGoogle Scholar | open url image1

Houter NC, Pons TL (2005) Gap size effects on photoinhibition in understorey saplings in tropical rainforest. Plant Ecology 179, 43–51.
Crossref | GoogleScholarGoogle Scholar | open url image1

Johnson GN (1993) The dissipation of excess excitation energy in British plant species. Plant, Cell & Environment 16, 673–679.
Crossref | GoogleScholarGoogle Scholar | open url image1

Jordan S, Simon C, Polhemus D (2003) Molecular systematics and adaptive radiation of Hawaii’s endemic damselfly genus Megalagrion (Odonata: Coenagrionidae). Systematic Biology 52, 89–109.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Kamaluddin M, Grace J (1992) Acclimation in seedlings of a tropical tree, Bischofia javanica, following a stepwise reduction in light. Annals of Botany 69, 557–562. open url image1

Kambysellis MP , Craddock EM (1997) Ecological and reproductive shifts in the diversification of the endemic Hawaiian Drosophila. In ‘Molecular evolution and adaptive radiation’. (Eds TJ Givnish, KJ Sytsma) pp. 475–509. (Cambridge University Press: New York)

Kornyeyev D, Logan BA, Tissue DT, Allen RD, Holaday AS (2006) Compensation for PSII photoinactivation by regulated non-photochemical dissipation influences the impact of photoinactivation on electron transport and CO2 assimilation. Plant & Cell Physiology 47, 437–446.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Krause GH (1988) Photoinhibition of photosynthesis. An evaluation of damaging and protective mechanisms. Physiologia Plantarum 74, 566–574.
Crossref | GoogleScholarGoogle Scholar | open url image1

Lammers TG (1990) Campanulaceae. In ‘Manual of the flowering plants of Hawai’i’. (Eds WL Wagner, DR Herbst, SH Sohmer) pp. 420–489. (Bishop Museum Press: Honolulu)

Lee DW (1989) Canopy dynamics and light climates in a tropical moist deciduous forest in India. Journal of Tropical Ecology 5, 65–79. open url image1

Lee H-Y, Chow WS, Hong Y-N (1999) Photoinactivation of photosystem II in leaves of Capsicum annuum. Physiologia Plantarum 105, 376–383.
Crossref | GoogleScholarGoogle Scholar | open url image1

Lee HY, Hong YN, Chow WS (2001) Photoinactivation of photosystem II complexes and photoprotection by non-functional neighbours in Capsicum annuum L. leaves. Planta 212, 332–342.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Lindqvist C, Motley TJ, Jeffrey JJ, Albert VA (2003) Cladogenesis and reticulation in the Hawaiian endemic mints (Lamiaceae). Cladistics 19, 480–495.
Crossref | GoogleScholarGoogle Scholar | open url image1

Logan BA, Barker DH, Demmig-Adams B, Adams WW (1996) Acclimation of leaf carotenoid composition and ascorbate levels to gradients in the light environment within an Australian rainforest. Plant, Cell & Environment 19, 1083–1090.
Crossref | GoogleScholarGoogle Scholar | open url image1

Logan BA, Barker DH, Adams WW, Demmig-Adams B (1997) The response of xanthophyll cycle-dependent energy dissipation in Alocasia brisbanensis to sunflecks in a subtropical rainforest. Australian Journal of Plant Physiology 24, 27–33. open url image1

Logan BA, Demmig-Adams B, Adams WW (1998a) Antioxidants and xanthophyll cycle-dependent energy dissipation in Cucurbita pepo L. and Vinca major L. upon a sudden increase in growth PPFD in the field. Journal of Experimental Botany 49, 1881–1888.
Crossref | GoogleScholarGoogle Scholar | open url image1

Logan BA, Demmig-Adams B, Adams WW, Grace SC (1998b) Antioxidants and xanthophyll cycle-dependent energy dissipation in Cucurbita pepo L. and Vinca major L. acclimated to four growth PPFDs in the field. Journal of Experimental Botany 49, 1869–1879.
Crossref | GoogleScholarGoogle Scholar | open url image1

Logan BA, Adams WW, Demmig-Adams B (2007) Avoiding common pitfalls of chlorophyll fluorescence analysis under field conditions. Functional Plant Biology 34, 853–859.
Crossref | GoogleScholarGoogle Scholar | open url image1

Lovelock CE, Jebb M, Osmond CB (1994) Photoinhibition and recovery in tropical plant species: response to disturbance. Oecologia 97, 297–307. open url image1

Lovelock CE, Kursar TA, Skillman JB, Winter K (1998) Photoinhibition in tropical forest understorey species with short- and long-lived leaves. Functional Ecology 12, 553–560.
Crossref | GoogleScholarGoogle Scholar | open url image1

Montgomery RA, Givnish TJ (2008) Adaptive radiation of photosynthetic physiology in the Hawaiian lobeliads: dynamic photosynthetic responses. Oecologia 155, 455–467.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Mulkey SS, Pearcy RW (1992) Interactions between acclimation and photoinhibition of photosynthesis of a tropical forest understorey herb, Alocasia macrorrhiza, during simulated gap formation. Functional Ecology 6, 719–729.
Crossref | GoogleScholarGoogle Scholar | open url image1

Nepokroeff M, Sytsma KJ, Wagner WL, Zimmer EA (2003) Reconstructing ancestral patterns of colonization and dispersal in the Hawaiian understory tree genus Psychotria (Rubiaceae): a comparison of parsimony and likelihood approaches. Systematic Biology 52, 820–838.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Niinemets U, Bilger W, Kull O, Tenhunen JD (1998) Acclimation to high irradiance in temperate deciduous trees in the field: changes in xanthophyll cycle pool size and in photosynthetic capacity along a canopy light gradient. Plant, Cell & Environment 21, 1205–1218.
Crossref | GoogleScholarGoogle Scholar | open url image1

Öquist G, Chow WS, Anderson JM (1992) Photoinhibition of photosynthesis represents a mechanism for the long-term regulation of photosystem II. Planta 186, 450–460.
Crossref | GoogleScholarGoogle Scholar | open url image1

Pearcy RW, Osteryoung K, Randall D (1982) Carbon dioxide exchange characteristics of C4 Hawaiian Euphorbia species native to diverse habitats. Oecologia 55, 333–341.
Crossref | GoogleScholarGoogle Scholar | open url image1

Piano F, Craddock EM, Kambysellis MP (1997) Phylogeny of the island populations of the Hawaiian Drosophila grimshawi complex: evidence from combined data. Molecular Phylogenetics and Evolution 7, 173–184.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Robichaux RH (1984) Variation in the tissue water relations of 2 sympatric Hawaiian Dubautia species and their natural hybrid. Oecologia 65, 75–81.
Crossref | GoogleScholarGoogle Scholar | open url image1

Robichaux RH, Canfield JE (1985) Tissue elastic properties of 8 Hawaiian Dubautia species thet differ in habitat and dipolid chromosome number. Oecologia 66, 77–80.
Crossref | GoogleScholarGoogle Scholar | open url image1

Robichaux RH, Pearcy RW (1980) Environmental characteristics, field water relations, and photosynthetic responses of C4 Hawaiian Euphorbia species from contrasting habitats. Oecologia 47, 99–105.
Crossref | GoogleScholarGoogle Scholar | open url image1

Robichaux RH, Pearcy RW (1984) Evolution of C3 and C4 plants along an environmental moisture gradient: patterns of photosynthetic differentiation in Hawaiian Scaevola and Euphorbia species. American Journal of Botany 71, 121–129.
Crossref | GoogleScholarGoogle Scholar | open url image1

Robichaux RH, Carr GD, Liebman M, Pearcy RW (1990) Adaptive radiation of the Hawaiian silversword alliance (Compositae: Madiinae)—ecological morphological, and physiological diversity. Annals of the Missouri Botanical Garden 77, 64–72.
Crossref | GoogleScholarGoogle Scholar | open url image1

Rock JF (1919) A monographic study of the Hawaiian species of the tribe Lobeliodeae, family Campanulaceae. Memoirs of the Bernice Pauahi Bishop Museum 7, 1–394. open url image1

Rundell RJ, Holland BS, Cowie RH (2004) Molecular phylogeny and biogeography of the endemic Hawaiian Succineidae (Gastropoda: Pulmonata). Molecular Phylogenetics and Evolution 31, 246–255.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Sakai AK , Weller SG , Wagner WL , Soltis PS , Soltis DE (1997) Phylogenetic perspectives on the evolution of dioecy: adaptive radiation in the endemic Hawaiian genera Scheidea and Alsinodendron. In ‘Molecular evolution and adaptive radiation’. (Eds TJ Givnish, KJ Sytsma) pp. 455–473. (Cambridge University Press: New York)

Schluter D (2000) ‘The ecology of adaptive radiation.’ (Oxford University Press: Oxford)

Schneider H, Ranker TA, Russell SJ, Cranfill R, Geiger JMO, Aguraiuja R, Wood KR, Grundmann M, Kloberdanz K, Vogel JC (2005) Origin of the endemic fern genus Diellia coincides with the renewal of Hawaiian terrestrial life in the Miocene. Proceedings of the Royal Society B: Biological Sciences 272, 455–460.
Crossref | GoogleScholarGoogle Scholar | open url image1

Shaw KL (1996) Sequential radiations and patterns of speciation in the Hawaiian cricket genus Laupala inferred from DNA sequences. Evolution 50, 237–255.
Crossref | GoogleScholarGoogle Scholar | open url image1

Valladares F, Pearcy RW (1997) Interactions between water stress, sun-shade acclimation, heat tolerance and photoinhibition in the schlerophyll Heteromeles arbutifolia. Plant, Cell & Environment 20, 25–26.
Crossref | GoogleScholarGoogle Scholar | open url image1

Valladares F, Allen MT, Pearcy RW (1997) Photosynthetic responses to dynamic light under field conditions in six tropical rainforest shrubs occurring along a light gradient. Oecologia 111, 505–514.
Crossref | GoogleScholarGoogle Scholar | open url image1

Watling JR, Robinson SA, Woodrow IE, Osmond CB (1997) Responses of rainforest understorey plants to excess light during sunflecks. Australian Journal of Plant Physiology 24, 17–25. open url image1

Weller SG, Sakai AK, Rankin AE, Golonka A, Kutcher B, Ashby KE (1998) Dioecy and the evolution of pollination systems in Schiedea and Alsinidendron (Caryophyllaceae: Alsinoideae) in the Hawaiian Islands. American Journal of Botany 85, 1377–1388.
Crossref | GoogleScholarGoogle Scholar | open url image1